Non-linear elasticity and short-range mechanical coupling govern the rate and symmetry of Hydra mouth opening

Extreme deformations in epithelial tissues play a key role in animal development and physiology. Often these deformations are produced by short range forces that need to be coordinated to generate a globally symmetric deformation. We used the mouth opening behavior in Hydra to study how tissue geometry allows coordination of local forces to achieve rapid and symmetrical global tissue deformation. Hydra is a freshwater polyp that rips a hole (“mouth”) in its head epithelium for ingestion, egestion, and osmoregulation. Within 1-2 minutes, the mouth opening becomes tens of cell diameters. Hydra’s circular mouth opening suggests globally coordinated cell deformation, but it is produced by stochastic contractile forces acting only over 2-3 cell diameters. Using a combination of experiments to alter the tissue geometry and boundary, and mathematical modelling, we showed how mechanical constraints imposed by tissue geometry promote the global symmetry of the mouth opening. We further show how mouth opening is coordinated through nearest-neighbor mechanical signaling in the absence of neuronal and chemical signaling.